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Complex Spatio-Temporal Distribution and Genogeographic Affinity of Mitochondrial DNA Haplogroups in 24,216 Danes

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Complex Spatio-Temporal Distribution and Genogeographic Affinity of Mitochondrial DNA Haplogroups in 24,216 Danes bioRxiv preprint doi: https://doi.org/10.1101/148494; this version posted June 10, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Complex spatio-temporal distribution and genogeographic affinity of mitochondrial DNA haplogroups in 24,216 Danes Jonas Bybjerg-Grauholm1*, Christian M Hagen1*, Vanessa F Gonçalves2, Marie Bækvad-Hansen1, Christine S Hansen1, Paula L Hedley1, Jørgen K Kanters3, Jimmi Nielsen4, Michael Theisen1, Ole Mors5, James Kennedy2, Thomas D Als6, Alfonso B Demur7, Thomas M Werge7, Merete Nordentoft8, Anders Børglum6, Preben Bo Mortensen9, David M Hougaard1 & Michael Christiansen1,3# 1) Department for Congenital Disorders, Statens Serum Institut, Copenhagen, Denmark 2) Centre for Addiction and Mental Health, University of Toronto, Toronto, Canada 3) Department of Biomedical Sciences, University of Copenhagen, Copenhagen, Denmark 4) Aalborg Psychiatric Hospital. Aalborg University Hospital, Aalborg, Denmark 5) Department of Clinical Medicine, Aarhus University, Århus, Denmark 6) Institute of Medical Genetics, Aarhus University, Århus, Denmark 7) Mental Health Centre, Sct Hans, Capital Region of Denmark, Denmark 8) Mental Health Centre, Capital Region of Denmark, Denmark 9) Center for Register Research, Institute of Economics, Aarhus University, Århus, Denmark The study was conducted under the auspices of the iPSYCH study (www.iPSYCH.au.dk) *JG and CMH contributed equally to the study. Key words: mitochondrial DNA, haplogroup, population genetics, energy metabolism Running title: mtDNA haplogroups in 24,216 Danes #Correspondence: Professor, chief physician, Michael Christiansen, FRCPath, MD Department for Congenital Disorders, Statens Serum Institut And Department of Biomedical Sciences, University of Copenhagen. E-mail: [email protected]; Phone: +4520720463. 1 bioRxiv preprint doi: https://doi.org/10.1101/148494; this version posted June 10, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Abstract Mitochondrial DNA (mtDNA) haplogroups (hgs) are evolutionarily conserved sets of mtDNA SNP- haplotypes with characteristic geographical distribution. Associations of hgs with disease and physiological characteristics have been reported, but have frequently not been reproducible. Using 418 mtDNA SNPs on the PsychChip (Illumina), we assessed the spatio-temporal distribution of mtDNA hgs in Denmark in DNA isolated from 24,642 geographically un-biased dried blood spots (DBS), collected from 1981 to 2005 through the Danish National Neonatal Screening program. Geno-geographic affinity (ancestry background) was established with ADMIXTURE using a reference of 100K+ autosomal SNPs in 2,248 individuals from nine populations. The hg distribution was typically Northern European, and hgs were highly variable based on median-joining analysis, suggesting multiple founder events. Considerable heterogeneity and variation in autosomal geno- geographic affinity was observed. Thus, individuals with hg H exhibited 95 %, and U hgs 38.2 % - 92.5 %, Danish ancestry. Significant clines between geographical regions and rural and metropolitan populations were found. Over 25 years, macro-hg L increased from 0.2 % to 1.2 % (p = 1.1*E-10), and M from 1 % to 2.4 % (p = 3.7*E-8). Hg U increased among the R macro-hg from 14.1 % to 16.5 % (p = 1.9*E-3). Geno-geographic affinity, geographical skewedness, and sub-hg distribution suggested that the L, M and U increases are due to immigration. The complex spatio-temporal dynamics and geno-geographic heterogeneity of mtDNA in the Danish population reflect repeated migratory events and, in later years, net immigration. Such complexity may explain the often contradictory and population-specific reports of mito-genomic association with disease. 2 bioRxiv preprint doi: https://doi.org/10.1101/148494; this version posted June 10, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Introduction Mitochondria are subcellular organelles responsible for oxidative phosphorylation (OXPHOS), producing ~ 80% of the ATP in eukaryotic cells1, apoptosis and cell-cycle regulation2, redox- and calcium homeostasis3 as well as intracellular signaling4. Each mitochondrion contains 2 - 10 copies of a 16.6 kb double-stranded mtDNA containing 37 genes5. Thirteen genes code for proteins in the five enzyme complexes conducting OXPHOS, whereas twenty-two genes code for tRNAs and two for rRNAs, all involved in intra-mitochondrial translation6. The mitochondrial proteome comprises approximately 1200 proteins7; 8, of which mtDNA genes encode ~ 1%. The mtDNA is maternally inherited9, exhibits a high mutation rate10, and does not undergo recombination5. Genetic variants in mtDNA – as well as variants in the nuclear genes encoding the mitochondrial proteome - have been associated with disease11; 12 13. More than 150 mitochondrial syndromes14 have been associated with more than 300 variants7; 15. Geographically and population specific lineages of mtDNA, haplogroups (hgs), have become fixed17, through the processes of random genetic drift and selection as the human populations dispersed throughout the world16. The advent of high throughput DNA sequencing technology, as well as implementation of biobanking technologies18, has enabled the construction of a high-resolution phylogenetic matrilineal mtDNA tree, Figure 119. Mitochondrial hgs have been assigned a role as disease modifiers5. Particularly in neurological degenerative diseases such as Alzheimer’s disease 20-23 and Parkinson’s disease 23-25, but also in psychiatric disease26 and cardiac diseases such as hypertrophic27; 28 and ischemic cardiomyopathy29. 3 bioRxiv preprint doi: https://doi.org/10.1101/148494; this version posted June 10, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Supporting a role as disease modifiers, some mtDNA hgs have specific physiological characteristics, e.g. reduced or increased ATP synthesis rates30; 31, and variation in methylation status of genes involved in inflammation and signaling32; 33. The association of mtDNA SNPs and hgs with both diseases and functional characteristics of mitochondria, has led to a pathogenic paradigm34 where variation in mitochondrial function is considered to be of paramount importance for development of disease. Specific hgs have also been associated with longevity35 and likelihood of being engaged in endurance athletic activities36. The clinical presentation of diseases caused by specific mtDNA variants depends, in some cases, on the hg background37. However, some of these studies are contradictory, either because they have been too poorly powered38, have not been carefully stratified with respect to sex, age, geographical background39 or population admixture40, or have used small areas of recruitment risking “occult” founder effects41. To circumvent some of these problems a recent large study on mtDNA SNPs identified a number of SNPs that were associated with several degenerative diseases42, however, the study pooled sequence information from a large geographical area, without correcting for potential population sub-structure. Most countries have a complex history with repeated migrations43 and several bottle-necks caused by disease, war and emigration44; 45. These demographic events are reflected in the fine scale genetic structure within sub-populations46. However, the significance of such events to countrywide mtDNA hg distribution has not yet been assessed. As mtDNA interact functionally with the nuclear genome, it is paramount to ensure that specific mtDNA hgs – which are a marker of matrilineal genetic origin – do not represent population sub-structure at the genomic level. In theory, mtDNA is inherited independently of the nuclear genome, but population admixture and 4 bioRxiv preprint doi: https://doi.org/10.1101/148494; this version posted June 10, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. geographic isolation may result in linkage disequilibrium between mtDNA and the nuclear genome. Such a linkage disequilibrium might interfere with genetic association analysis. Here we demonstrate the complexity of the spatio-temporal dynamics and genogeographic affinity of mtDNA hgs in 24,216 Danes, which were sampled at birth during a 25-year period. This number represents 1.6 % of the population. The sampling material was dried blood spots (DBSs) obtained as part of the Danish Neonatal Screening Program47, the very nature of which makes sampling geographically un-biased. Array analysis was performed using the PsychChip (Illumina, CA, USA) typing 588,454 variants. 5 bioRxiv preprint doi: https://doi.org/10.1101/148494; this version posted June 10, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Materials and Methods Ethics statement This is a register-based cohort study solely using data from national health registries. The study was approved by the Scientific Ethics Committees of the Central Denmark Region (www.komite.rm.dk) (J.nr.:
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